the Science of the

Total lkixmunent

The Scienceof the Total Environment 203(1997) 83-91

Arsenic and heavy metal contamination of soil and

vegetation around a copper mine in Northern Peru

Jaume Beth”, Charlotte Poschenrieder b, Mere? Llugany b, Juan BarceGby*,

P. Tumea, F.J. Tobias”, J.L. Barranzuelac, E.R. Vksquez”
aChair of Soil Science, Faculty of Biology, University of Barcelona, Avda. Diagonal 645, E-08028 Barcelona, Spain
bPlant Physiolocy Laboratory Science Faculty, Autonomous University of Barcelona, E-08193 Bellaterra, Spain
‘Section of Industrial Processes and Analysis, Engineering Faculty, Piura University, Piura, Peru

Received 13 February 1997;accepted8 May 1997

Abstract

At present,very little information is availableon either the environmentalimpact or the biogeochemistryof mine
sitesin Latin America. Here we present preliminary resultson contamination of soilsand plants around a copper
mine in the Andes of Northern Peru. Plants and soilswere sampledat six sites ranging from low (Sl) to high
phytotoxicity (S6); sampleswere analysedfor concentrationsof As and heavy metals.Stepwisemultiple regression
analysiswas usedin order to determinethe soil factors that significantly influenced As and metal availability. High
As and Cu concentrationsin soil extracts (ammoniumacetate-EDTA), in addition to low pH and high Al availability,
seemto be the most important soil factors that limit plant performance around the mine. A high organic matter
content favoured Cu and Al extractability. Nevertheless,phytotoxicity was more intense at siteswith low organic
matter concentrations.Unusually high concentrationsof As and metal concentrationswere detected in leavesof
somespecies(e.g. in Bidenscynapiifolia up to 1430pg/g dry wt. As, 437 Zn, 620 Cu, 6510Al and 5.7% Fe) while
others (e.g. Eriochlou ramosa)more effectively restricted metal transport to the shoots.These plant speciesseem
interesting for future investigationson both metal tolerance mechanismsand revegetation of contaminatedsoilsat
the numerousmine siteslocated at high altitudes in equatorial regions. 0 1997Elsevier ScienceB.V.

Keywords: Arsenic; Copper; Heavy metal; Metal tolerance; Soil contamination;Mining

*Corresponding author.Tel.: f34 3 5811267;

fax: +34 3
5812003;
e-mail:j-barcelo@cc.uab.es

0048-9697/97/%17.00 0 1997 Elsevier Science B.V. All rights reserved.

PII SOO48-9697(97) 00336-8
x4 J. Beth et al. / The Science of the Total Environment
1. Introduction
Mining activities have a considerable impact on
the environment. Besides the local disturbance of
the soil profile and structure, a more widespread
contamination of soils, vegetation and water
courses by toxic concentrations of metals and
metalloids can occur (Down and Stocks, 1977;
Wilmoth et al., 1991). The type of metal contami-
nation around copper mines mainly depends on
the composition of the mined Cu ore and the
accompanying gangue. Increased concentrations
(0.1% or higher) of Cu, Zn, Pb, Co, Ni, Cd, As
and others have been reported from several sites
and those high metal concentrations in soils are
known to have strong uptake selection by the
natural vegetation (Ernst, 1974 and references
therein).
The Peruvian Andes are very rich in ore de-
posits (Cardozo and Cedillo, 19901 and an impor-
tant mining activity has developed there. How-
ever. at present very little information is available
on either the environmental impact or the bio-
geochemistry of the mine sites.
Native farmers, living downstream of the cop-
per mine investigated in this study, have observed
unidentified toxic effects in natural vegetation
and crop plants. Health problems of the inhabi-
tants and cattle in the zone downstream of the
mine have been attributed to the ingestion of
drinking water and plants contaminated by the
mining activity. As far as we know, no chemical
analysis of contaminated soils and plants around
the mine has been reported. Several factors make
field work in this zone extremely difficult. Among
these. the difficulty of accessibility to the mine,
remotely located at an altitude of 2600 m in the
Andes, deserves special mention.
The main objectives of the present investiga-
tion were not only to identify the metals and
metalloids that may be responsible for phytotoxic
effects in this zone, but also to provide the first
results which may contribute to the very small
volume of biogeochemical data available for Latin
America in comparison to that recorded for North
America. Europe or Africa (Brooks, 1993).
203 (1997) 83-91
2. Materials and methods
2.1. Site description and sampling
The copper mine is located in the Canchaque
district of the department of Piura (Northern
Peru) in the Western Andes (lat 045’S; long
79”45’W) at an altitude of 2600 m (Fig. 1). The
main Cu ore extracted in the mine is chalcopyrite
(CuFeS,) with a Cu content of 0.6-3%. Associ-
ated with the chalcopyrite, arsenopyrite (FeAsS),
pyrite (FeS,) and other sulphide minerals are also
present. The main gangue minerals are black
tourmaline [XY,Z,(B0,)3Si,0,8(0,0H,F),l
where usually X is Na, Ca or a vacancy, Y is Al,
Li, Fe2+, Fe3+ and many other cations and Z is
Al, Mg and Fe3+, quartz (SiO,) and actinolite
[Ca,(Mg,Fe),Si,O,,(OH,F),]. Among the acces-
sory minerals, bomite, molybdenite and wol-
framite are present (G6mez La Torre, unpub-
lished results).
The climate diagram (Fig. 2), drawn with dam
from the nearest, comparable meteorological sta-
tion that provides reliable temperature and pre-
cipitation data (Huarmaca, lat 05”34’09”S; long
79”31’23”W, altitude 2194 m), is typical for equa-
torial orobiomes, i.e. zones at high altitudes
(Walter and Breckle, 1984) with almost constant
monthly mean temperatures. Rainfall is highest
in summer (January-March), while the drought
period occurs in late autumn (June) and winter
(July-September). The predominant vegetation in
the zone is the Andean rainforest formed by
shrubs and trees (Yuglans sp., Cnctors callicarpae-
folius, Erythrina sp., Ficus sp., etc.), epiphytic
lichens (Tillandsia usneoides) and orchids.
The local environmental impact of the mining
activity is clearly observed by changes in species
composition (absence of trees) and density of the
vegetation cover around the mine. Due to the
difficulties mentioned in the introduction, an ex-
haustive sampling was impossible and six sam-
pling sites with apparently different degrees of
contamination were chosen by eye, according to
the following selection criterions: vegetation
 J. Beth et al. / The Science of the Total Environment 203 (1997) 83-91 85

SOUTH AMERICA

Fig. 1. Localization of the copper mine (Mina Turmalina, Canchaque).

cover, soil colour and texture, phytotoxicity symp- analysed using ammonium acetate-EDTA
toms in the form of chlorosis and stunting, dis- (NH,OAc-EDTA) extracts according to Cottenie
tance to the mine and predominant direction of et al. (1979). Concentrations of Al, As, Ba, Cd,
wind. At each site, numbered Sl to S6 from Cr, Cu, Fe, Mn, Ni, Pb, Sr and V in the extracts
apparently low to high contamination, surface (10 were determined by ICP-ES (Yvon JY38-VHR).
cm depth) soil samples were taken in triplicate. A Limits of determination (99% confidence inter-
variable number of plant species (l-5) were col- val) were 100 kg/l for As, Pb and Al and 25
lected at each site: Biderzs cynapiifolia HPK, pg/l for Cd, Z n, Mn and Fe. Arsenic was de-
Asteraceae (Sl, S2, S3); Micoti Zutescens(Bonpl.) termined at line 189.042, where no interference
DC, Melastomataceae (Sl, S6); SteZZuriacuspida with argon plasma occurs.
Willd, Caryophyllaceae 64); Puspulum mcemo-
sum, Poaceae (S4, S5); Paspalum tuberosum Mez 2.3. Plant analysis
(S5); Eupatorium sp., Asteraceae 65); Eriochloa
ramosa (Retz.) Kunze, Poaceae (S5); S’rI+zria
All plant material was carefully washed with
grandis (Pers) ST I-U, Caryophyllaceae (S5). tap water, followed by 0.01 N HCl and distilled
water. The concentrations of metals in the tap
2.2. Soil anatysis water were below EC guideline values for drinking
water and did not significantly contribute to metal
After removal of large stones, air dried soil contamination of the plant samples. The dried
samples were sieved (2 mm) and analysed for (65°C) plant material was then wet ashed
physical properties, pH (H,O), organic matter, (HNO,/HClO,/H,SO, = 1O:l:l) and analysed by
C/N ratio and electrical conductivity by standard ICP-ES for Al, As, B, Cd, Cr, Cu, Fe, Mg, Mn, Ni,
methods. Aqua regia extracts were used for the Pb and P. Titanium concentrations in acid
estimation of pseudototal soil metals (ISO/CD (HNO,/HClO,/H,SO, = 1O:l:l) digests of soil
114661, while the so-called available fraction was samples and plant material were analysed by ICP-
86 J. Beth et al. / l%e Science of the Total Environment 203 (1997) 83-91

Hua- (MS4 m)

MONTH
Fig. 2. Climate diagram from the nearest, comparable meteorological station (Huarmaca). Note that the months shown on the
abscissa are numbered from July (month 1) to June (month 12), because the meteorological station is located in the southern
hemisphere.

ES and used as an indicator of soil contamination Table 1

of plant material according to Car-y et al. (1986). Selected properties of soils sampled around the copper mine
Soil and plant Ti concentrations ranged from 0.08 Sample Site Sand Silt Clay pH E.C.’ 0.M.’ C/N
to 0.52% and from 22 to 460 pug/g, respectively. (%) (%I (%I (H,O) (dS/m) (%o) (%o)
The individual value for contamination by soil
Sl 16.7 44.7 38.5 5.22 0.10 11.0 12.8
particles of each leaf sample was taken for cor-
s2 19.2 55.3 25.5 4.95 0.12 23.4 16.0
recting its metal concentration and the leaf metal s3 25.4 43.3 31.3 4.42 0.15 15.6 14.8
concentrations shown are corrected values. s4 85.4 10.1 4.5 5.86 0.36 2.3 11.0
s5 48.9 28.7 22.4 5.19 0.38 4.1 10.7
2.4. Statistics S6 86.9 6.9 6.2 3.33 0.65 2.3 13.8
’ Electrical conductivity.
Ail soil and plant analysis data are for triplicate ’ Organic matter.
samples from each site. Stepwise multiple regres-
sion analysis was performed (Sokal and Rolf, 1981)
in order to describe the factors that may explain organic matter content (Table 1). The organic
both the increased metal availability in the soil matter content and pH values were lowest and
extracts and the increased metal concentrations the proportion of coarse soil fraction was highest
in the plant material. Only factors that were on the mine spoil heap (site S6).
significant at the P I 0.05 level were used for the At all sample sites pseudototal (aqua regia) and
multiple regression equations. extractable Ba, Cr, Ni, Sr and V concentrations
(data not shown) were below the range of values
3. Results above which toxicity is considered to be possible
(Kabata-Pendias and Pendias, 1992). Potentially
The soils from different sampling sites at the phytotoxic total As, Cd and Cu concentrations
copper mine highly differed in texture, pH and were found in most of the soil samples (Table 2).
 .I. Beth et al. /The Science of the Total Environment 203 (1997) 83-91 87

Table 2 creased with pH values. Soil texture largely de-

Pseudototal (aqua regia extract) arsenic and metal concentra- termined As extractability, while extractable con-
tions in soil sampled around the copper mine.
centrations of Al and Cu increased with soil or-
Sample site As Concentrations (mg/kgf % ganic matter content (Table 4).
Cd Zn Cu Pb Mn Fe Al Plants from all sites exhibited above the ‘nor-
mal’ (Alloway, 1995) average leaf As and Cu
Sl 143 8.9 56 69 196 213 5.95 9.14 concentrations (Table 5). Unusually high leaf Fe
s2 1921 125 224 1874 285 356 5.09 6.66 and Al concentrations were also found on most
s3 2790 183 235 801 156 714 4.05 5.25
s4 5247 352 772 5270 194 965 4.14 0.91 sites. Average leaf concentrations of Zn and Mn
s5 7670 499 284 2118 341 317 5.80 4.93 were slightly above ‘normal’ at sites S2 and S3,
S6 3052 201 276 1549 87 508 2.81 1.10 respectively. At all sites, leaf Cd concentrations
were below detection limits (< 1.2 pg/g> and Pb,
Ni, Cr and B concentrations were not above ‘nor-
Excepting Pb, Fe and Al, the lowest metal and As mal’ levels (data not shown).
total soil concentrations were found at Site 1. Significant linear relationships between average
Even at this site, As and Cd concentrations were leaf As or Cu concentrations and extractable soil
above ‘normal’ total concentrations (Alloway, As or Cu were found (Table 4). The average leaf
1995). However, in the NH,OAc-EDTA extracts Zn concentrations were not significantly corre-
from this site As and Cd were not detectable lated with any of the soil factors determined in
(Table 3). The highest extractable concentrations the study, but a significant relation with leaf Cu
of As, Cd, Mn and Fe were found on the highly concentrations was established. Leaf Al concen-
acidic (pH 3.3) spoil heap at site S6 (Table 3), trations were also positively related to leaf Cu;
while extracts from soils at sites S2 and S4 ren- however, low soil pH had a more important in-
dered the highest concentrations for Cu and Mn, fluence as indicated by the standardized form of
respectively.
the regression equation (Table 4). Leaf Mn con-
The soil factors that significantly influenced
centrations were positively influenced by the
extractable As and metal concentrations in the pseudototal soil Mn concentrations and, to a
soils are shown in the linear stepwise multiple lesser extent, by the clay content of soils.
regression analysis in Table 4. Only the ex- Different plant species differed largely in As
tractability of Zn was significantly related to its and metal leaf concentrations. Among the
total soil concentration. Total Fe concentrations Poaceae growing at the site with the highest total
negatively influenced Mn extractability, while that As soil concentration (S5), Eriochloa ramosu ac-
of Fe was positively related to total soil As. Low
cumulated significantly lower As concentrations
pH favoured extractability of As, Fe and Al. Con- than Paspalum species, P. racemosum and P.
trastingly, Mn concentrations in the extracts in- tuberosum (Table 6). Bidens cynapiifolia from Site
3 exhibited considerably higher leaf As concen-
Table 3 trations than Eupatorium sp., the other Asteracea
NH,OAc-EDTA extractable arsenic and metal concentrations
(mg/kg) in soils around the copper mine. (n.d., not de- species found at Site 5. The most remarkable
tectable) species differences were observed for Al, Fe and
Mn leaf concentrations (Table 6).
Sample site As Concentrations (mg/kg)
Cd Zn Cu Pb Mn Fe Al
4. Discussion
Sl < 0.25 < 0.05 0.08 0.48 0.61 0.83 10 98
s2 0.95 0.07 0.84 53 1.6 1.0 35 119
s3 4.2 0.14 1.5 6.0 1.7 3.4 53 158 Both soil and plant mineral analysis data indi-
s4 7.0 0.26 5.9 16 4.9 10 28 7.9 cate that high As and Cu concentrations, in addi-
s5 3.9 0.12 1.0 36 1.6 0.50 52 44 tion to low pH leading to high Al availability, are
S6 13 3.8 1.4 6.0 0.61 7.1 71 15 probably the most important chemical factors
88 J. Beth et al. /The Science of the Total Environment 203 (1997) 83-91

Table 4
Soil (NH,OAc-EDTA extractable) and leaf concentrations as a function of some physical and chemical soil properties. Subscripts
tot, ext, and leaf refer to soil pseudototal, soil NH,OAc-EDTA extractable and leaf metal concentrations, respectiveiy

Linear stepwise multiple Standardized form Multiple R2 P

regression equationa

Soil extractable
As = 24.50 - 2.86 pH - 0.27 clay - 0.51 pH - 0.75 clay 0.9323 < 0.02
Zn = - 0.80 + 0.0084 Zn,,, 0.9699 < 0.001
Mn = 6.11 - 4.17 Ferot + 3.53 pH - 1.28 Fe,,, + 0.78 pH 0.9184 < 0.01
Fe = 134.12 + 0.0051 As,, - 22.85 pH - 0.92 pH + 0.62 Astor 0.9592 < 0.01
Cu = 11.62 - 0.51 Al,, + 4.44 O.M. - 1.60 Al,,, + 1.84 O.M. 0.8156 < 0.07
Al = 4.70 + 6.57 O.M. 0.7583 < 0.03

Leaf concentrations
As = 470.79 + 95.69 As,,r 0.6976 < 0.04
Cu = 41.47 + 8.91 Cuext 0.8031 < 0.02
Mn = - 1119 + 2.02 Mn,,, + 30.08 clay 1.17 Mn,,, + 0.84 clay 0.8920 < 0.05
Al = 14360 - 2820 pH + 9.66 Culeaf - 0.80 pH + 0.65 Culeaf 0.9357 < 0.02
Zn = 84.52 + 0.57 Culeaf 0.6519 < 0.01
a Only factors that were significant at the P I 0.05 level were included in the regression equations.

Table 5 plants. However, in the soils with total As concen-

Average As, P and metal concentrations in leaves of plants
sampled around the copper mine trations far beyond normal background levels, the
- available As fraction was much more influenced
Sample site ( /G/d (mg/d by soil texture and pH than by the total soil As
As Zn Cu Mn Al Fe P concentration. The strong negative influence of
soil clay content on As availability and phytotoxic-
Sl 111 90 41 357 674 3.40 1.78
s2 649 437 617 209 6509 0.58 1.76 ity has been explained by the high correlation
s3 1433 338 100 1448 2273 1.66 1.37 between the soil contents of clay and amorphous
54 1063 257 202 808 407 4.46 1.83 Fe and Al oxides and by the observation that Fe
S5 760 92 194 318 329 1.54 1.41 and Al oxides strongly adsorb As (Wauchope and
S6 1651 131 142 226 6800 4.97 2.13
.--- McDowell, 1984; Adriano, 1986). The highest ex-
tractable As concentrations in this study were
found at sites with the lowest clay contents (S4
limiting plant performance around the copper
mine. Although inorganic and waste forms of As and S6).
Acidification, due to oxidation of the sulphidic
are much less toxic than organic sources, the soil
As concentrations found here are much higher tailings (Marshman et al., 19951, further en-
than the average toxicity threshold of 40 mg/kg hanced As availability (sites S3 and S6). With
established for crop plants (Sheppard, 1992). In- strongly acidic pH the As-binding species such as
creased As concentrations in soils and plants af- Fe and Al oxycompounds become more soluble
fected by mining activities have been frequently (O’Neill, 1995) and As extractability increased.
reported (Wild, 1974, Porter and Peterson, 1975; The range of shoot As concentrations found in
De Koe, 1994). the species of this study were within those re-
The high leaf As concentrations and the sig- ported for Agrostis species from acidic mine soils
nificant correlation between NH,OAc-EDTA ex- from the Jales gold mine in Portugal (De Koe,
tractable soil As and leaf As concentrations (Ta- 1994) and from mine wastes in the U.K. (Porter
ble 4) found in this study also show that the and Peterson, 1975).
arsenopyrite derived soil As is largely available to Highest As concentrations were found in dead
 J. Beth et al. /The Science of the Total Environment 203 (1997) 83-91 89

Table 6
Range of As and metal concentrations in selected plant species sampled at different sites around the copper mine. Mean values
(n-3) for species sampled at only one site are given

Concentrations ( pg/g dry wt.) (%I

As zn CU Mn Al Fe

Miconia lurcccm~ 112-1650 58-131 37-142 226-442 6410-6800 1.85-4.97

Bidens cyqkifdia 130-1430 89-437 36-620 209-412 618-6510 0.58-5.67
Paspalwn racemown 1530~5280a 275-604 188-1880a 1210-1490a 489-12125a 6.68-7.08
Pqmkun tubemsum 1130 61 300 40 183 0.96
spe?gu&lriagmndis 1175 92 334 68 1036 2.60
steua?i4l cuspida 589 239 275 400 326 2.24
Eupathorium sp. 461 140 105 1285 26 1.50
Eriochiou mmosa 317 61 88 65 317 0.82
a High values of upper limit due to presence of dead leaves in the samples; these sample values were not used for calculation of
average values in Table 5.

leaves of Paspa&r rucemo~um (Table 6). How-
ever, even in green leaves As concentrations were
substantially higher than in roots, where up to
500 ppm As were found (data not shown). Similar
results have been reported for Agr0sti.s can&
and it has been suggested that accumulation of
As in older leaves is a means for avoiding toxic
concentrations in growing tissues (De Koe et al.,
1988). This tolerance strategy seems restricted to
only some Poacean species because all other
species from our study, including the Poaceaen
Eriochloa rumosa, and also Agrostis castellana
from the Jales gold mine in Portugal described by
De Koe et al. (19881, accumulated more As in
roots (data not shown) than in shoots.
Taking into account both the toxicity of As to
man and cattle (Hapke, 1991; L&nard, 1991) and
the halo effect of As tUNeill, 19951, which may
cause increased soil As concentrations in a waste
area around the mine as well as As contamination
of river sediments and water, the health problems
observed downstream from the Canchaque cop-
per mine may be attributed to As. Analysis of
drink@ water and crop soil should be performed
to co&m this.
High Cu and Al concentrations are expected to
be mostly a local problem to the vegetation in the
near vicinity of the mine. The Cu and Al leaf
concentrations found in most of the species of
this study were unusually high, even for metallo-
phytes. Although foliar absorption of trace ele-
ments from the atmosphere cannot be excluded
(Ormrod, 19841, the correction of leaf metal con-
centrations for soil particle contamination may
justify the assumption that most of the metal was
taken up by roots and translocated to the leaves.
Soil extractability of both Cu and Al was largely
favoured by soil organic matter (Table 4). Both
0.1 and Al form organic complexes which seem to
be less phytotoxic than the free metal ion species
(Bloom et al., 1979; Stevenson and Fitch, 1981).
The activity of both free Al and Cu ions increases
in acid substrates with low organic matter content
(Ross, 1994). Accordingly, at the acid spoil heap
at site S6, with lower extractable Cu and Al
concentrations and lower organic matter content
than at site S2, plant growth was visibly more
restricted than at site S2. However, high As avail-
ability, proton toxicity and unfavourable soil
structure may also be responsible for the bad
plant performance at site S6, in addition to Al
and Cu toxicity.
Average leaf Al and Zn concentrations at the
different sites were significantly related to leaf
Cu. This may suggest a common uptake and
transport strategy for these metals. However, con-
sidering the leaf metal concentrations of the indi-
vidual species it seems clear that the plant species
growing around the copper mine have developed
different strategies to cope with the high soil
metal concentrations. Leaf concentrations of As,
Cu and Al linearly increased with extractable soil
metal concentrations in Bidens cynapiifolia; i.e. B.
cynapii~oliu behaved as an indicator species sensu
90 J. Beth et al. /The Science of the Total Environment
Baker (1981). Tolerance of unusually high leaf
metal concentrations must imply effective inter-
nal detoxification mechanisms. However, the
absence of B. cynapiifolia from the apparently
more phytotoxic sites S4, S5 and S6, suggest that
this tolerance strategy was not sufficient to over-
come the extreme conditions on the soils with low
organic matter content. Among the species found
on these sites only Miconia lutescens and, to a
lesser extent, Spegularia grandis accumulated high
Al concentrations in green leaves, while all other
species seemed to exclude Al at least from the
shoots or, as P. racemosum, accumulated it in
dead leaves. Paspalum tuberosum, Spergularia
grandis and Stellaria cuspida seem able to translo-
cate considerable Cu concentrations to the shoots,
while Miconia lutescens, Eupatotium sp. and Eri-
ochloa ramosa were more effective in excluding
Cu from shoots. Eupatorium sp. also effectively
excluded Al, while the Mn leaf concentration was
considerably increased in this species. If further
investigations using controlled metal supply in
nutrient solutions confirm these tolerance strate-
gies, these species may be a very interesting mate-
rial not only for the investigation of heavy metal
tolerance mechanisms, but also for the revegeta-
tion of the numerous mine sites located at high
altitudes in equatorial regions.
Acknowledgements
The authors are very grateful to Prof. Dr.
Freddy Zufiiga for classifying the plant material
and to the Spectroscopy Service of Barcelona
University for technical assistance. Travel expen-
ses and lodging of Prof. Dr. Beth were provided
by the Autonomous Government of Catalonia
and the University of Piura, respectively. This
work was partially supported by the Spanish Gov-
ernment (DGICYT PB 94-0738-CO2-01).
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